INBREEDING DEPRESSION AND ITS EVOLUTIONARY CONSEQUENCES

The harmful effects of close inbreeding have been noticed for many centuries (34, 35, 165). With the rise of Mendelian genetics, it was realized that the main genetic consequence of inbreeding is homozygosis (165, Ch. 2). Two main theories were early proposed to account for inbreeding depression and its converse, heterosis (the increase in vigor observed in an F1 between two inbred lines). These are the overdominance and partial dominance hypotheses, discussed in more detail below. Research into this question has continued up to the present, and this is one of the topics that we discuss. Darwin (35, 36) was the first to point out that the evident adaptations of many plants for ensuring outcrossing could be understood in terms of the selective advantage of avoiding inbreeding depression. We review the evidence that the evolution of breeding systems of animals and plants has been significantly influenced by the occurrence of inbreeding depression. In order to do this, we consider the contemporary genetic theory of inbreeding depression and heterosis, and the experimental data concerning the strength of inbreeding depression. We emphasize data and theory relevant to natural, rather than domesticated, populations as we are chiefly concerned to evaluate the evolutionary significance of inbreeding depression. We do not attempt to give a complete bibliography of this very extensive field but try to concentrate on what seem to be the most significant findings in relation to this aim.

[1]  R. Ward,et al.  Population genetics of polymorphisms in Cardiff newborn. Relationship between blood group and allozyme heterozygosity and birth weight. , 1985, Human Heredity.

[2]  B. Charlesworth The cost of sex in relation to mating system. , 1980, Journal of theoretical biology.

[3]  D. Soltis,et al.  Polyploidy and Breeding Systems in Homosporous Pteridophyta: A Reevaluation , 1987, The American Naturalist.

[4]  D. Charlesworth Androdioecy and the evolution of dioecy , 1984 .

[5]  R. Lloyd, Mating systems and genetic load in pioneer and non‐pioneer Hawaiian Pteridophyta * , 1974 .

[6]  D. Walter Is there Disruptive Selection for Self-Fertilization? , 1986, The American Naturalist.

[7]  F. R. Ganders The biology of heterostyly , 1979 .

[8]  David G. Lloyd,et al.  Benefits and handicaps of sexual reproduction. , 1980 .

[9]  J. Thomson Selection for Outcrossing, Sexual Selection, and the Evolution of Dioecy in Plants , 1981, The American Naturalist.

[10]  T. Aide THE INFLUENCE OF WIND AND ANIMAL POLLINATION ON VARIATION IN OUTCROSSING RATES , 1986, Evolution; international journal of organic evolution.

[11]  D. Houle,et al.  Homozygous and Hemizygous Viability Variation on the X Chromosome of DROSOPHILA MELANOGASTER. , 1985, Genetics.

[12]  D. Schemske BREEDING SYSTEM AND HABITAT EFFECTS ON FITNESS COMPONENTS IN THREE NEOTROPICAL COSTUS (ZINGIBERACEAE) , 1983, Evolution; international journal of organic evolution.

[13]  W. Schull,et al.  The effects of inbreeding on Japanese children , 1965 .

[14]  J. Haldane,et al.  The association of characters as a result of inbreeding and linkage. , 1949, Annals of eugenics.

[15]  T. Givnish Outcrossing Versus Ecological Constraints in the Evolution of Dioecy , 1982, The American Naturalist.

[16]  E. Klekowski,et al.  Reproductive biology of the Pteridophyta: 1. General considerations and a study of Onoclea sensibilis L. , 1968 .

[17]  M. C. Grant,et al.  Associations Among Protein Heterozygosity, Growth Rate, and Developmental Homeostasis , 1984 .

[18]  C. Strobeck,et al.  Temporal variation of the mating system in a natural population of jack pine. , 1985, Genetics.

[19]  T. Nagylaki A model for the evolution of self-fertilization and vegetative reproduction. , 1976, Journal of theoretical biology.

[20]  J. Patterson,et al.  Evolution in the genus Drosophila , 1952 .

[21]  H. F. Robinson,et al.  Statistical genetics and plant breeding. , 1963 .

[22]  J. Crow,et al.  Mutations affecting fitness in Drosophila populations. , 1977, Annual review of genetics.

[23]  J. M. Smith The Sex Habit in Plants and Animals , 1977 .

[24]  S. Austad,et al.  When Should Animals Tolerate Inbreeding? , 1986, The American Naturalist.

[25]  D. Levin INBREEDING DEPRESSION AND PROXIMITY‐DEPENDENT CROSSING SUCCESS IN PHLOX DRUMMONDII , 1984, Evolution; international journal of organic evolution.

[26]  M. J. Lawrence,et al.  Variation in wild populations of Papaver dubium VI. Dominance relationships for genes controlling metrical characters , 1973, Heredity.

[27]  M. V. Price,et al.  Pollen dispersal and optimal outcrossing in Delphinium nelsoni , 1979, Nature.

[28]  V. Singh,et al.  Mating Systems and Distribution in some Tropical Ferns , 1977 .

[29]  E. Franklin Survey of mutant forms and inbreeding depression in species of the family Pinaceae. , 1970 .

[30]  S. Jain,et al.  AN ECOLOGICAL GENETIC STUDY OF GYNODIOECY IN LIMNANTHES DOUGLASII (LIMNANTHACEAE) , 1984 .

[31]  S. Strauss Heterosis at Allozyme Loci under Inbreeding and Crossbreeding in PINUS ATTENUATA. , 1986, Genetics.

[32]  Comstock Re,et al.  The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. , 1948 .

[33]  G. Muenchow An S-Locus Model for the Distyly Supergene , 1981, The American Naturalist.

[34]  D. Mccauley,et al.  INBREEDING AND THE RATE OF SELF‐FERTILIZATION IN A GRAPE FERN, BOTRYCHIUM DISSECTUM , 1985 .

[35]  P. Harvey,et al.  Inbreeding: Do animals avoid incest? , 1986, Nature.

[36]  F. Sorensen,et al.  Inbreeding depression in height, height growth, and survival of Douglas-fir, ponderosa pine, and noble fir to 10 years of age. , 1982 .

[37]  D. Lloyd Selection of Combined Versus Separate Sexes in Seed Plants , 1982, The American Naturalist.

[38]  E. Franklin Genetic Load in Loblolly Pine , 1972, The American Naturalist.

[39]  C. W. Cotterman,et al.  A calculus for statistico-genetics , 1940 .

[40]  D. Schoen,et al.  The selection of cleistogamy and heteromorphic diaspores , 1984 .

[41]  R. B. Campbell The interdependence of mating structure and inbreeding depression. , 1986, Theoretical population biology.

[42]  G. Sprague,,et al.  Heterosis in Maize: Theory and Practice , 1983 .

[43]  P. Hedrick,et al.  Genetic Polymorphism in Heterogeneous Environments , 1976 .

[44]  D. G. Lloyd,et al.  The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy , 1986 .

[45]  S. Jain,et al.  The Genetics of Inbreeding Populations , 1968 .

[46]  C. Perrins,et al.  Inbreeding and dispersal in the great tit , 1978, Nature.

[47]  A. Jacquard The Genetic Structure of Populations , 1974 .

[48]  E. Klekowski EVIDENCE AGAINST GENETIC SELF‐INCOMPATIBILITY IN THE HOMOSPOROUS FERN PTERIDIUM AQUILINUM , 1972, Evolution; international journal of organic evolution.

[49]  E. Klekowski Genetic load and soft selection in ferns , 1982, Heredity.

[50]  D. Sperlich,et al.  Genetic Load and Viability Distribution in Central and Marginal Populations of DROSOPHILA SUBOBSCURA. , 1977, Genetics.

[51]  S. Barrett,et al.  VARIATION AND EVOLUTION OF BREEDING SYSTEMS IN THE TURNERA ULMIFOLIA L. COMPLEX (TURNERACEAE) , 1987, Evolution; international journal of organic evolution.

[52]  J. Crow,et al.  A Comparison of the Effect of Lethal and Detrimental Chromosomes from Drosophila Populations. , 1960, Genetics.

[53]  J. Jinks Biometrical Genetics of Heterosis , 1983 .

[54]  W. Shields Philopatry, Inbreeding, and the Evolution of Sex , 1983 .

[55]  D. Waller,et al.  GENETIC CONSEQUENCES OF OUTCROSSING IN THE CLEISTOGAMOUS ANNUAL, IMPATIENS CAPENSIS. I. POPULATION‐GENETIC STRUCTURE , 1987, Evolution; international journal of organic evolution.

[56]  Mandy J. Haldane,et al.  A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[57]  Baker Hg Reproductive methods as factors in speciation in flowering plants. , 1959 .

[58]  W. G. Hill,et al.  Measuring Selection in Natural Populations , 1977 .

[59]  J. M. Smith Evolution of sex , 1975, Nature.

[60]  Rory A. Fisher,et al.  AVERAGE EXCESS AND AVERAGE EFFECT OF A GENE SUBSTITUTION , 1941 .

[61]  A. Wilton,et al.  X-chromosomal heterosis in Drosophila melanogaster. , 1979, Genetical research.

[62]  A. Bateman Self-incompatibility systems in angiosperms , 1952, Heredity.

[63]  G. Muller-Starck Reproductive systems in conifer seed orchards. I. Mating probabilities in a seed orchard of Pinus sylvestris L. , 1982 .

[64]  S. Weller,et al.  CYTOGEOGRAPHIC EVIDENCE FOR THE EVOLUTION OF DISTYLY FROM TRISTYLY IN THE NORTH AMERICAN SPECIES OF OXALIS SECTION IONOXALIS , 1976 .

[65]  G. Furnier,et al.  Mating system in natural populations of Jeffrey pine , 1986 .

[66]  R. Lumaret,et al.  Reproductive capacities in the sexual forms of the gynodioecious species Thymus vulgaris L. , 1978 .

[67]  D. Schemske POPULATION STRUCTURE AND LOCAL SELECTION IN IMPATIENS PALLIDA (BALSAMINACEAE), A SELFING ANNUAL , 1984, Evolution; international journal of organic evolution.

[68]  M. Uyenoyama INBREEDING AND THE COST OF MEIOSIS: THE EVOLUTION OF SELFING IN POPULATIONS PRACTICING BIPARENTAL INBREEDING , 1986, Evolution; international journal of organic evolution.

[69]  A. Brown Enzyme polymorphism in plant populations , 1979 .

[70]  P. Smouse THE FITNESS CONSEQUENCES OF MULTIPLE‐LOCUS HETEROZYGOSITY UNDER THE MULTIPLICATIVE OVERDOMINANCE AND INBREEDING DEPRESSION MODELS , 1986, Evolution; international journal of organic evolution.

[71]  M. Feldman,et al.  The Evolution of Self-Fertilization in Plants: A Population Genetic Model , 1984, The American Naturalist.

[72]  C. Cockerham,et al.  Detrimental genes with partial selfing and effects on a neutral locus. , 1974, Genetical research.

[73]  E. Klekowski POPULATIONAL AND GENETIC STUDIES OF A HOMOSPOROUS FERN—OSMUNDA REGALIS , 1970 .

[74]  D. P. Fowler,et al.  Population studies of white spruce. II. Natural inbreeding and relatedness among neighboring trees. , 1984 .

[75]  Charles Darwin,et al.  The Effects of Cross and Self Fertilisation in the Vegetable Kingdom , 1972 .

[76]  M. Begon,et al.  The genetics of Drosophila subobscura populations , 1980, Heredity.

[77]  J. Sved An estimate of heterosis in Drosophila melanogaster. , 1971, Genetical research.

[78]  G. Ledyard Stebbins,et al.  Variation and Evolution in Plants , 1951 .

[79]  B. Charlesworth,et al.  Population genetics of partial male-sterility and the evolution of monoecy and dioecy , 1978, Heredity.

[80]  D. Schoen RELATIVE FITNESSES OF SELFED AND OUTCROSSED PROGENY IN GILIA ACHILLEIFOLIA (POLEMONIACEAE) , 1983, Evolution; international journal of organic evolution.

[81]  D. G. Lloyd,et al.  Some Reproductive Factors Affecting the Selection of Self-Fertilization in Plants , 1979, The American Naturalist.

[82]  H. Whitehouse Multiple-allelomorph incompatibility of pollen and style in the evolution of the angiosperms. , 1950 .

[83]  P. Hedrick GENETIC POLYMORPHISM IN HETEROGENEOUS ENVIRONMENTS: A DECADE LATER , 1986 .

[84]  J H Gillespie,et al.  A general model to account for enzyme variation in natural populations. V. The SAS--CFF model. , 1978, Theoretical population biology.

[85]  B. Weir,et al.  Digenic descent measures for finite populations , 1977 .

[86]  U. Gullberg,et al.  Allozyme variation in Scots pine (Pinus sylvestris L.) in Sweden , 1985 .

[87]  R. W. Allard Principles of Plant Breeding , 1960 .

[88]  J H Gillespie,et al.  A general model to account for enzyme variation in natural populations. , 1974, Genetics.

[89]  S. Wright Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions , 1977 .

[90]  P. Greenwood Mating systems, philopatry and dispersal in birds and mammals , 1980, Animal Behaviour.

[91]  F. Ayala,et al.  A population cage test for heterosis in Drosophila pseudoobscura. , 1970, Genetics.

[92]  R. Lewontin,et al.  The Genetic Basis of Evolutionary Change , 2022 .

[93]  Ralph RILEYs THE INFLUENCE OF THE BREEDING SYSTEM ON THE GENECOLOGY OF THLASPI ALPESTRE L. , 1956 .

[94]  B. Charlesworth,et al.  A Model for the Evolution of Dioecy and Gynodioecy , 1978, The American Naturalist.

[95]  R. Sarvas Investigations on the flowering and seed crop of Pinus silvestris. , 1962 .

[96]  M. A. Farris,et al.  POPULATION DENSITY, OUTCROSSING RATE, AND HETEROZYGOTE SUPERIORITY IN PONDEROSA PINE , 1984, Evolution; international journal of organic evolution.

[97]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[98]  M. Bulmer The Mathematical Theory of Quantitative Genetics , 1981 .

[99]  D. Lindgren,et al.  Gene Dispersion and Selfing Frequency in a Seed-Tree Stand of Pinus Sylvestris (L.) , 1985 .

[100]  M. Kimura,et al.  An introduction to population genetics theory , 1971 .

[101]  R. Lande,et al.  THE EVOLUTION OF SELF‐FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. II. EMPIRICAL OBSERVATIONS , 1985, Evolution; international journal of organic evolution.

[102]  B. Charlesworth,et al.  The Maintenance and Breakdown of Distyly , 1979, The American Naturalist.

[103]  B. Charlesworth,et al.  Breeding system evolution in Primula vulgaris and the role of reproductive assurance , 1986, Heredity.

[104]  Robert C. Elston,et al.  Genealogical and Genetic Structure. , 1982 .

[105]  D. Soltis,et al.  ELECTROPHORETIC EVIDENCE FOR INBREEDING IN THE FERN BOTRYCHIUM VIRGINIANUM (OPHIOGLOSSACEAE) , 1986 .

[106]  J. Crow,et al.  The influence of epistasis on homozygous viability depression in Drosophila melanogaster. , 1969, Genetics.

[107]  W. Ewens Selection and Mutation , 1968 .

[108]  Elizabeth A. Thompson,et al.  Genealogical and genetic structure , 1984 .

[109]  R. Lande,et al.  THE EVOLUTION OF SELF‐FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. I. GENETIC MODELS , 1985, Evolution; international journal of organic evolution.

[110]  D. Waller DIFFERENCES IN FITNESS BETWEEN SEEDLINGS DERIVED FROM CLEISTOGAMOUS AND CHASMOGAMOUS FLOWERS IN IMPATIENS CAPENSIS , 1984, Evolution; international journal of organic evolution.

[111]  H. F. Robinson,et al.  Estimates of Genetic Variances and Level of Dominance in Maize. , 1964, Genetics.

[112]  J. Haldane,et al.  A mathematical theory of natural and artificial selection , 1926, Mathematical Proceedings of the Cambridge Philosophical Society.

[113]  D. Charlesworth On the Nature of the Self-Incompatibility Locus in Homomorphic and Heteromorphic Systems , 1982, The American Naturalist.

[114]  C. Strobeck Partial selfing and linkage: the effect of a heterotic locus on a neutral locus. , 1979, Genetics.

[115]  J. Franklin,et al.  Self-pollination effects on seed and seedling traits in Noble Fir. , 1976 .

[116]  B. Charlesworth,et al.  A Model for the Evolution of Distyly , 1979, The American Naturalist.

[117]  R. Comstock,et al.  ANALYSIS OF GENETIC VARIABILITY IN CORN WITH REFERENCE TO PROBABLE EFFECTS OF SELECTION , 1955 .

[118]  K. Holsinger DISPERSAL AND PLANT MATING SYSTEMS: THE EVOLUTION OF SELF‐FERTILIZATION IN SUBDIVIDED POPULATIONS , 1986, Evolution; international journal of organic evolution.

[119]  F. Sorensen Embryonic Genetic Load in Coastal Douglas-Fir, Pseudotsuga menziesii var. Menziesii , 1969, The American Naturalist.

[120]  S. Jain BREEDING SYSTEM IN LIMNANTHES ALBA: SEVERAL ALTERNATIVE MEASURES , 1978 .

[121]  M. Clegg,et al.  Estimation of mating system parameters when outcrossing events are correlated. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[122]  D. Charlesworth THE EVOLUTION AND BREAKDOWN OF TRISTYLY , 1979, Evolution; international journal of organic evolution.

[123]  B. Charlesworth,et al.  The evolution and breakdown of S-allele systems , 1979, Heredity.

[124]  N. Morton,et al.  AN ESTIMATE OF THE MUTATIONAL DAMAGE IN MAN FROM DATA ON CONSANGUINEOUS MARRIAGES. , 1956, Proceedings of the National Academy of Sciences of the United States of America.

[125]  E. Klekowski MUTATIONAL LOAD IN CLONAL PLANTS: A STUDY OF TWO FERN SPECIES , 1984, Evolution; international journal of organic evolution.